Hydrobiologia

, Volume 342, Issue 0, pp 355–365 | Cite as

Biomanipulation in shallow lakes: state of the art

  • Martin R. Perrow
  • Marie-Louise Meijer
  • Piotr Dawidowicz
  • Hugo Coops
Article

Abstract

The current state of biomanipulation was the subject of muchdiscussion at Shallow Lakes ‘95. This led to a workshop focusing onthe factors influencing the establishment of macrophytes and themechanisms responsible for their stability followingbiomanipulation. The purpose of the current paper is to distilcurrent knowledge on biomanipulation in shallow lakes gleaned fromdiscussions at the conference and recent literature.Biomanipulation should be used in the theoretical context of twoaltemative stable equilibria, as the extreme perturbation requiredto move from a phytoplankton dominated state to one dominated bymacrophytes. Understanding the nature of the factors and mechanismsresponsible for turbid water, is critical if biomanipulation is tobe appropriate. We suggest that with sufficient information,particular components of the fish community may be targeted andprecise figures for removal, designed to exceed critical thresholdvalues, may be set. Without this knowledge, a ‘play-safe’ strategyshould be adopted and at least 75% of the fish removed. Stockingwith piscivores may be a useful additional measure to fish removal.The principal objective of biomanipulation in shallow lakes is togenerate a period of clear water of sufficient length to allowmacrophytes to establish. To this aim, as well as for technicalreasons, biomanipulation is best undertaken in winter and earlyspring to generate clear water as early as possible in the season.In the cases where grazing is important, this coincides with thespring peak of Daphnia spp. Biomanipulation may have to berepeated if macrophytes do not colonise effectively within thefirst season. The factors responsible for the lag in response ofmacrophytes in some cases and the potential mechanisms contributingto the maintenance of clear water in macrophyte beds are discussed.From empirical data sets from many lakes, both a relative increasein the piscivorous fish stock and a reduction in nutrient levelsare thought to be important in stabilising the system in thelong-term. Whether biomanipulation may lead to alternativeequilibria (i.e. high diversity macrophyte communities withpiscivorous fish at high P) is unknown. Further study ofexceptional cases, theoretical modelling and development andanalysis of more long-term (>10 years) case histories isrecommended.

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. Agami, M. & Y. Waisel, 1986. The role of mallard ducks (Anas platyrhynchos) in distribution and germination of seeds of the submerged hydrophyte Najas marinaL. Oecologia 68: 473–475.Google Scholar
  2. Anderson, M. G. & J. B. Low, 1976. Use of Sago pondweed on the Delta Marsh, Manitoba. J. Wildl. Mgmt 40: 233–242.Google Scholar
  3. Backx, J. J. G. M. & M. P. Grimm, 1994. Mass removal of fish from Lake Wolderwijd, The Netherlands. Part II: Implementation phase. In Cowx, I. G. (ed.), Rehabilitation of Freshwater Fisheries. Fishing News Books, Blackwell Scientific Publications Ltd., Oxford, England.Google Scholar
  4. Balls, H., B. Moss & K. Irvine, 1989. The loss of submerged plants with eutrophication I. Experimental design, water chemistry, aquatic plant and phytoplankton biomass in experiments carried out in ponds in the Norfolk Broadland. Freshwat. Biol. 22: 71–87.Google Scholar
  5. Benndorf, J., 1992. The control of the indirect effects of biomanipulation. In Sutcliffe, D. W. & J. G. Jones (eds), Eutrophication: Research and Application to Water Supply. Freshwater Biological Association, Far Sawrey, Ambleside, Cumbria, England.Google Scholar
  6. Benndorf, J.& U. Miersch, 1991. Phosphorus loading and efficiency of biomanipulation. Verh. int. Ver. Limnol. 24: 2482–2488.Google Scholar
  7. Berg, S., E. Jeppesen & M. Søndergaard, 1997. Pike (Esox luciusL.) stocking as a biomanipulation tool 1. Effects on the fish population in Lake Lyng, Denmark. Hydrobiologia 342/343: 311–318.Google Scholar
  8. Berg, S., E. Jeppesen, M. Sondergaard & E. Mortensen, 1994. Environmental effects of introducing whitefish, Coregonus lavaretus (L.) in Lake Ring. Hydrobiologia 275/276: 71–79.Google Scholar
  9. Blindlow, I., G. Andersson, A. Hargeby & S. Johansson, 1993. Long term pattern of alternative stable states in two shallow eutrophic lakes. Freshwat. Biol. 30: 159–167.Google Scholar
  10. Breukelaar, A. W., E. H. R. R. Lammens, J. G. P. Klein Breteler & I. Tatrai, 1994. Effects of benthivorous beam (Abramis brama L.) and carp (Cyprinus carpioL.) on sediment resuspension and concentrations of nutrients and chlorophyll a. Freshwat. Biol. 32: 113–121.Google Scholar
  11. Bronmark, C., 1994. Effects of tench and perch on interactions in a freshwater, benthic food chain. Ecology 75: 1818–1828.Google Scholar
  12. Bronmark, C., C. A. Paszkowski, W. M. Tonn & A. Hargeby, 1995. Predation as a determinant of size structure in populations of crucian carp (Carassius carassius) and tench (Tinca tinca). Ecol. Freshwat. Fish 4: 85–92.Google Scholar
  13. Bronmark, C. & S. E. B. Weisner, 1992. Indirect effects of fish community structure on submerged vegetation in shallow, eutrophic lakes: an alternative mechanism. Hydrobiologia 243/244: 293–301.Google Scholar
  14. Brooks, J. L. & S. I. Dodson, 1965. Predation, body size, and composition of plankton. Science 150: 28–35.Google Scholar
  15. Carvalho, L., 1994. Top-down control of phytoplankton in a shallow hypertrophic lake: Little Mere (England). Hydrobiologia 275/276: 53–63.Google Scholar
  16. Cook, M. F. & E. P. Bergersen, 1988. Movements, Habitat Selection, and Activity Periods of Northern Pike in Eleven Mile Reservoir, Colorado. Trans. am. Fish. Soc. 117: 495–502.Google Scholar
  17. Coops, H. & R.W. Doef, 1996. Submerged vegetation development in two shallow, eutrophic lakes. Hydrobiologia 340: 115–120.Google Scholar
  18. Cryer, M., G. Peirson & C. R. Townsend, 1986. Reciprocal interactions between roach Rutilus rutilus, and zooplankton in a small lake: Prey dynamics and fish growth and recruitment. Limnol. Oceanogr. 31: 1022–1038.Google Scholar
  19. Dawidowicz, P., 1990. Effectiveness of phytoplankton control by large-bodied and small-bodied zooplankton. Hydrobiologia 200/201: 43–47.Google Scholar
  20. de Bernardi, R. & G. Giussani, 1990. Are blue-green algae a suitable food for zooplankton? An overview. Hydrobiologia 200/201: 29–41.Google Scholar
  21. de Nie, A. W., 1987. The decrease in aquatic vegetation in Europe and its consequences for fish populations. EIFAC Occasional Paper 19. FAO, Rome, 88 pp.Google Scholar
  22. Denny, P., 1987. Mineral cycling by wetland plants–a review. Arch. Hydrobiol. Beih. Ergebn. Limnol. 27: 1–25.Google Scholar
  23. Diehl, S., 1993. Effects of habitat structure on resource availability, diet and growth of benthivorous perch, Perca fluviatilis. Oikos 67: 403–414.Google Scholar
  24. Dorgelo, J. & M. Heykoop, 1985. Avoidance of macrophytes by Daphnia longispina. Verh. int. Ver. Limnol. 22: 3369–3372.Google Scholar
  25. Driessen, O., B. Pex & H. Tolkamp, 1993. Restoration of a lake: First results and problems. Verh. int. Ver. Limnol. 25: 617–621.Google Scholar
  26. Eklov, P. & S. F. Hamrin, 1989. Predatory efficiency and prey selection: interactions between pike Esox lucius, perch Perca fluviatilis and rudd Scardinius erythrophthalmus. Oikos 56: 149–156.Google Scholar
  27. Esler, D., 1989. An assessment of American coot herbivory of Hydrilla. J. Wildl. Mgmt 1147–1149.Google Scholar
  28. Faafeng, B. A. & A. Braband, 1990. Biomanipulation of a small urban lake-removal of fish exclude bluegreen blooms. Verh. int. Ver. Limnol. 24: 597–602.Google Scholar
  29. Giles, N., 1992. Wildlife after gravel: twenty years of practical research by the Game Conservancy and ARC. Game Conservancy, Fordingbridge, UK.Google Scholar
  30. Gliwicz, Z. M., 1990. Why do cladocerans fail to control algal blooms? Hydrobiologia 200/201: 83–97.Google Scholar
  31. Gliwicz, Z. M. & A. Jachner, 1992. Diel migrations of juvenile fish: a ghost of predation past or present? Arch. Hydrobiol. 124: 385–410.Google Scholar
  32. Grimm, M. P., 1991. Water quantity management of Dutch polders, adversely affecting the recruitment of northern pike (Esox lucius L.). Verh. int. Ver. Limnol. 24: 2443–2445.Google Scholar
  33. Grimm, M. P., 1994. The influence of aquatic vegetation and population biomass on recruitment of 0+ and 1+ northern pike (Esox luciusL.). In Cowx, I. G. (ed.), Rehabilitation of Freshwater Fisheries. Fishing News Books, Blackwell Scientific Publications Ltd., Oxford, England.Google Scholar
  34. Grimm, M. P. & J. J. G. M. Backx, 1990. The restoration of shallow eutrophic lakes, and the role of northern pike, aquatic vegetation and nutrient concentration. Hydrobiologia 200/201: 557–566.Google Scholar
  35. Grimm, M. P. & J. J. G. M. Backx, 1994. Mass removal of fish from Lake Wolderwijd, The Netherlands. Part I: Planning and strategy of a large-scale biomanipulation project. In Cowx, I. G. (ed.), Rehabilitation of Freshwater Fisheries. Fishing News Books, Blackwell Scientific Publications Ltd., Oxford, England.Google Scholar
  36. Hambright, K. D., R. J. Trebatoski & R. W. Drenner, 1986. Experimental study of the impacts of Bluegill (Lepomis macrochirus) and Largemouth Bass (Micropterus salmoides) on pond community structure. Can. J. Fish. aquat. Sci. 43: 1171–1176.Google Scholar
  37. Hamrin, S. F., 1993. Lake restoration by cyprinid control in Satofta Bay (Lake Ringsjon). Verh. int. Ver. Limnol. 25: 487–493.Google Scholar
  38. Hanson, M. A. & M. G. Butler, 1994. Responses to food web manipulation in a shallow waterfowl lake. Hydrobiologia 279/280: 457–466.Google Scholar
  39. Hart, P. & S. F. Hamrin, 1988. Pike as a selective predator. Effects of prey size, availability, cover and pike jaw dimensions. Oikos 51: 220–226.Google Scholar
  40. Horppila, J. & T. Kairesalo, 1990. A fading recovery: the role of roach (Rutilus rutilusL.) in maintaining high phytoplankton productivity and biomass in LakeVesijarvi, southern Finland. Hydrobiologia 200/201: 153–165.Google Scholar
  41. Hosper, S. H. & E. Jagtman, 1990. Biomanipulation additional to nutrient control for restoration of shallow lakes in The Netherlands. Hydrobiologia 200/201: 523–534.Google Scholar
  42. Hosper, S. H. & M.-L. Meijer, 1993. Biomanipulation, will it work for your lake. A simple test for the assessment of chances for clear water, following drastic fish-stock reduction in shallow eutrophic lakes. Ecol. Engin. 2: 63–72.Google Scholar
  43. Irvine, K., B. Moss & H. Balls, 1989. The loss of submerged plants with eutrophication II. Relationships between fish and zooplankton in a set of experimental ponds, and conclusions. Freshwat. Biol. 22: 89–107.Google Scholar
  44. Jacobsen, L., M. R. Perrow, F. Landkildehus, M. Hjørne, T. L. Lauridsen & S. Berg, 1997. Interactions between piscivores, zooplanktivores and zooplankton in submerged macrophytes: preliminary observations from enclosure and pond experiments. Hydrobiologia 342/343: 197–205.Google Scholar
  45. James, W. F. & J. W. Barko, 1990. Macrophyte influences on the zonation of sediment accretion and composition in a north-temperate reservoir. Arch. Hydrobiol. 2: 129–142.Google Scholar
  46. Jeppesen, E., J. P. Jensen, P. Kristensen, M. Søndergaard, E. Mortensen, O. Sortkjör & K. Olrik, 1990a. Fish manipulation as a lake restoration tool in shallow, eutrophic, temperate lakes 2: threshold levels, long-term stability and conclusions. Hydrobiologia 200/201: 219–227.Google Scholar
  47. Jeppesen, E., J. P. Jensen, M. Søndegaard, T. Lauridsen, L. J. Pedersen & L. Jensen, 1997. Top-down control in freshwater lakes: the role of nutrient state, submerged macrophytes and water depth. Hydrobiologia 342/343: 151–164.Google Scholar
  48. Jeppesen, E., M. Søndergaard, E. Mortensen, P. Kristensen, B. Riemann, H. J. Jensen, J. P. Müller, O. Sortkjör, J. P. Jensen, K. Christoffersen, S. Bosselmann & E. Dall, 1990b. Fish manipulation as a lake restoration tool in shallow, eutrophic temperate lakes 1: cross-analysis of three Danish case-studies. Hydrobiologia 200/201: 205–218.Google Scholar
  49. Jupp, B. P. & D. H. N. Spence, 1977. Limitations of macrophytes in a eutrophic lake, Loch Leven. II. Wave action, sediments and waterfowl grazing. J. Ecol. 65: 431–446.Google Scholar
  50. Koch, M. S., I. A. Mendelssohn & K. L. McKee, 1990. Mechanism for the hydrogensulphide-induced growth limitation in wetland macrophytes. Limnol. Oceanogr. 35: 399–408.Google Scholar
  51. Lammens, E. H. R. R., P. J. Boesewinkel-de Bruyn, H. Hoogveld & E. van Donk, 1992. P-load, phytoplankton, zooplankton and fish stock in Loosdrecht Lake and Tjeukemeer: confounding effect of predation and food availability. Hydrobiologia 233: 87–95.Google Scholar
  52. Lammens, E. H. R. R., H. W. de Nie, J. Vijverberg & W. L. T. van Densen, 1985. Resources Partitioning and Niche Shifts of Bream (Abramis brama) and Eel (Anguilla anguilla) Mediated by Predation of Smelt (Osmerus eperlanus) on Daphnia hyalina. Can. J. Fish. aquat. Sci. 42: 1342–1351.Google Scholar
  53. Lammens, E. H. R. R., R. D. Gulati, M.-L. Meijer, E. van Donk, 1990. The first biomanipulation conference: a synthesis. Hydrobiologia 200/201: 619–628.Google Scholar
  54. Lauridsen, T. L., E. Jeppesen & F. Ostergaard Andersen, 1993. Colonization of submerged macrophytes in shallow fish manipulated Lake Vaeng: impact of sediment composition and waterfowl grazing. Aquat. Bot. 46: 1–15.Google Scholar
  55. Lauridsen, T. L., E. Jeppesen & M. Søndergaard, 1994. Colonization and succession of submerged macrophytes in shallow Lake Vaeng during the first five years following fish manipulation. Hydrobiologia 275/276: 233–242.Google Scholar
  56. Lauridsen, T. L. & D. M. Lodge, 1996. Avoidance by Daphnia magnaof fish and macrophytes: chemical cues and predator-mediated use of macrophyte habitat. Limnol. Oceanogr. 22: 805–810.Google Scholar
  57. Lauridsen, T. L., L. J. Pedersen, E. Jeppesen & M. Søndergaard (in press). The importance of macrophyte bed size for composition and horizontal migration of cladocerans in a shallow lake. J. Plankton Res.Google Scholar
  58. Mauck, W. L. & D. W. Coble, 1973. Vulnerability of Some Fishes to Northern Pike (Esox lucius) Predation. J. Fish. Res. Bd Can. 28: 957–969.Google Scholar
  59. Meijer, M.-L., A. W. Breukelaar & S. H. Hosper, 1994a. Mass removal of fish from LakeWolderwijd, The Netherlands. Part III: Effects on water quality. In I. G. Cowx (ed.), Rehabilitation of Freshwater Fisheries. Fishing News Books, Blackwell Scientific Publications Ltd., Oxford, England.Google Scholar
  60. Meijer, M.-L., M. W. de Haan, A. W. Breukelaar & H. Buiteveld, 1990. Is reduction of the benthivorous fish an important cause of high transparency following biomanipulation in shallow lakes? Hydrobiologia 200/201: 303–315.Google Scholar
  61. Meijer, M.-L. & H. Hosper, 1997. Effects of biomanipulation in the large and shallow Lake Wolderwijd, The Netherlands. Hydrobiologia 342/343: 335–349.Google Scholar
  62. Meijer, M.-L., E. Jeppesen, E. van Donk, B. Moss, M. Scheffer, E. Lammens, E. van Nes, J. A. van Berkum, G. L. de Jong, B. A. Faafeng & J. P. Jensen, 1994b. Long-term responses to fish-stock reduction in small shallow lakes: interpretation of five-year results of four biomanipulation cases in The Netherlands and Denmark. Hydrobiologia 275/276: 457–466.Google Scholar
  63. Meijer, M.-L., E. H. R. R. Lammens, A. J. P. Raat, J. G. P. Klein Breteler & M. P. Grimm, 1995. Development of fish communities in lakes after biomanipulation. Neth. J. aquat. Ecol. 29: 91–101.Google Scholar
  64. Mitchell, S. F., D. P. Hamilton, W. S. MacGibbon, P. K. B. Nayar & R. N. Reynolds, 1988. Interactions between phytoplankton, submerged macrophytes, black swans and zooplankton in a shallow lake. Int. Revue ges. Hydrobiol. 73: 145–170.Google Scholar
  65. Moss, B., 1990. Engineering and biological approaches to the restoration from eutrophication of shallow lakes in which aquatic plant communities are important components. Hydrobiologia 200/201: 367–377.Google Scholar
  66. Moss, B., J. H. Stansfield, K. Irvine, M. R. Perrow & G. L. Phillips, 1996. Progressive restoration of a shallow lake–a twelve-year experiment in isolation, sediment removal and biomanipulation. J. appl. Ecol. 33: 71–86.Google Scholar
  67. Ozimek, T., R. D. Gulati & E. van Donk, 1990. Can macrophytes be useful in biomanipulation of lakes? The Lake Zwemlust example. Hydrobiologia 200/201: 399–407.Google Scholar
  68. Pennak, R. W., 1973. Some evidence for aquatic macrophytes as repellents for a limnetic species of Daphnia. Int. Revue ges. Hydrobiol. 58: 569–576.Google Scholar
  69. Perrow, M. R., 1991. Reversing the effects of eutrophication upon fish communities: lessons from Broadland. In Lucas, M. C., I. Diack & L. Laird (eds), Interactions Between Fisheries and the Environment. Proceedings of the Institute of Fisheries Management, Nottingham, England: 111–125.Google Scholar
  70. Perrow, M. R., 1994. Practical aspects of the biomanipulation of fish populations. In Pitt, J.-A. & G. L. Phillips (eds), The Development of Biomanipulation Techniques & Control of Phosphorus Release from Sediments, EC LIFE project 92-3/UK/031, NRA Report No. 475/2/A. National Rivers Authority/Broads Authority, Bristol, UK.Google Scholar
  71. Perrow, M. R. & K. Irvine, 1992. The relationship between cladoceran body size and the growth of underyearling roach (Rutilus rutilus(L.)) in two shallow lowland lakes: a mechanism for density-dependent reductions in growth. Hydrobiologia 241: 155–161.Google Scholar
  72. Perrow, M. R., B. Moss & J. H. Stansfield, 1994. Trophic interactions in a shallow lake following a reduction in nutrient loading: a long term study. Hydrobiologia 275/276: 43–52.Google Scholar
  73. Perrow, M. R., J. Schutten, J. R. Howes, T. Holzer, F. J. Madgwick & A. J. D. Jowitt, 1997. Interactions between coot (Fulica atra) and submerged macrophytes: the role of birds in the restoration process. Hydrobiologia 342/343: 241–255.Google Scholar
  74. Persson, L., S. Diehl, L. Johansson, G. Andersson & S. F. Hamrin, 1991. Shifts in fish communities along the productivity gradient of temperate lakes-patterns and the importance of size-structured populations. J. Fish. Biol. 38: 281–293.Google Scholar
  75. Persson, L. & P. Eklov, 1995. Prey refuges affecting interactions between piscivorous perch and juvenile perch and roach. Ecology 76: 70–81.Google Scholar
  76. Phillips, G. L., D. F. Eminson & B. Moss, 1978. A mechanism to account for macrophyte decline in progressively eutrophicated freshwaters. Aquat. Bot. 4: 103–126.Google Scholar
  77. Phillips, G. L., M. R. Perrow & J. H. Stansfield, 1996. Manipulating the fish-zooplankton interaction in shallow lakes: a tool for restoration. In Greenstreet, S. P. R. & M. L. Tasker (eds), Aquatic Predators and Their Prey. Blackwell Scientific Publications Ltd., Oxford. England 174–183.Google Scholar
  78. Prejs, A., A. Martyniak, S. Boron, P. Hliwa & P. Koperski, 1994. Food web manipulation in a small, eutrophic Lake Wirbel, Poland: effect of stocking with juvenile pike on planktivorous fish. Hydrobiologia 275/276: 65–70.Google Scholar
  79. Reynolds, C. S., 1994. The ecological basis for the successful biomanipulation of aquatic communities. Arch. Hydrobiol. 130: 1–33.Google Scholar
  80. Ridley, H. N., 1930. The dispersal of plants throughout the world. L. Reeve & Co. Ashford, Kent, England. Scheffer, M., 1990. Multiplicity of stable states in freshwater systems. Hydrobiologia 200/201: 475–486.Google Scholar
  81. Scheffer, M., S. H. Hosper, M.-L. Meijer, B. Moss & E. Jeppesen, 1993. Alternative Equilibria in Shallow Lakes. TREE 8: 275–279.Google Scholar
  82. Scheffer, M., M. van der Berg, A. Breukelaar, C. Breukers, H. Coops, R. Doef & M.-L. Meijer, 1994. Vegetated areas with clear water in turbid shallow lakes. Aquat. Bot. 49: 193–196.Google Scholar
  83. Schriver, P., J. Bøgestrand, E. Jeppesen & M. Søndergaard, 1995. Impact of submerged macrophytes on fish-zooplankton-phytoplankton interactions: large-scale enclosure experiments in a shallow lake. Freshwat. Biol. 33: 255–270.Google Scholar
  84. Shapiro, J., 1990. Biomanipulation: the next phase-making it stable. Hydrobiologia 200/201: 13–27.Google Scholar
  85. Søndergaard, M., L. Bruun, T. L. Lauridsen, E. Jeppesen & T. Vindbaek Madsen, (in press). The impact of grazing waterfowl on submerged macrophytes: in situexperiments in a shallow eutrophic lake. Aquat. Bot.Google Scholar
  86. Søndergaard, M., E. Jeppesen & S. Berg, 1997. Pike (Esox lucius L.) stocking as a biomanipulation tool 2. Effects on the lower trophic levels in Lake Lyng, Denmark. Hydrobiologia 342/343: 319–325.Google Scholar
  87. Spencer, C. N. & D. L. King, 1984. Role of fish in Regulation of Plant and Animal Communities in Eutrophic Ponds. Can J. Fish. aquat. Sci. 41: 1851–1855.Google Scholar
  88. Stansfield, J. H. & M. R. Perrow, 1994. The influence of benthivorous fish upon benthic communities. In Pitt, J.-A. & G. L. Phillips (eds), The Development of Biomanipulation Techniques & Control of Phosphorus Release from Sediments, EC LIFE project 92-3/UK/031, NRA Report No. 475/2/A. National Rivers Authority/ Broads Authority, Bristol, UK.Google Scholar
  89. Stansfield, J. H., M. R. Perrow, L. D. Tench, A. J. D. Jowitt & A. A. L. Taylor, 1997. Submerged macrophytes as refuges for grazing Cladocera against fish predation: observations on seasonal changes in relation to macrophyte cover and predation pressure.Google Scholar
  90. Tatrai, I. & V. Istvanovics, 1986. The role of fish in the regulation of nutrient cycling in lake Balaton, Hungary. Freshwat. Biol. 16: 417–424.Google Scholar
  91. Tatrai, I., E. H. R. R. Lammens, A. W. Breukelaar & J. G. P. Klein Breteler, 1994. The impact of mature cyprinid fish on the composition and biomass of benthic macroinvertebrates. Arch. Hydrobiol. 131: 309–320.Google Scholar
  92. Ten Winkel, E. H. & J. T. Meulemans, 1984. Effects of fish upon submerged vgetation. Hydrobiol. Bull. 18: 157–158.Google Scholar
  93. Timms, R. M. & B. Moss, 1984. Prevention of growth of potentially dense phytoplankton populations by zooplankton grazing, in the presence of zooplanktivorous fish, in a shallow wetland system. Limnol. Oceanogr. 29: 472–486.Google Scholar
  94. Turner, A. M. & G. G. Mittelbach, 1992. Effects of grazer community composition and fish on algal dynamics. Can J. Fish. aquat. Sci. 49: 1908–1915.Google Scholar
  95. Underwood, G. J. C., J. D. Thomas & J. H. Baker, 1992. An experimental investigation of interactions in snail-macrophyte-epiphyte systems. Oecologia 91: 587–595.Google Scholar
  96. Van Brekum, J. A., M. Klinge & M. P. Grimm, 1995. Biomanipulation on the Duinigermeer: first results. Neth. J. aquat. Ecol. 29: 472–486.Google Scholar
  97. Van Densen, W. L. T., 1994. Predator enhancement in freshwater fish communities. In Cowx, I. G. (ed.), Rehabilitation of Freshwater Fisheries. Fishing News Books, Blackwell Scientific Publications Ltd., Oxford, England.Google Scholar
  98. Van der Vlugt, J. C., P. A. Walker, J. van der Does & A. J. P. Raat, 1992. Fisheries management as an additional lake restoration measure: biomanipulation scaling-up problems. Hydrobiologia 233: 213–225.Google Scholar
  99. Van Donk, E., E. de Deckere, J. G. P. Klein Breteler & J. T. Meulemans, 1994b. Herbivory by waterfowl and fish on macrophytes in a biomanipulated lake: effects on long-term recovery. Verh. int. Ver. Limnol. 25: 2139–2143.Google Scholar
  100. Van Donk, E., M. P. Grimm, R. D. Gulati, P. G. M. Heuts, W. A. de Kloet & L. van Liere, 1990a. First attempt to apply whole-lake food-web manipulation on a large scale in the Netherlands. Hydrobiologia 200/201: 291–301.Google Scholar
  101. Van Donk, E., M. P. Grimm, R. D. Gulati & J. P. G. Klein Breteler, 1990b. Whole-lake food-web manipulation as a means to study community interactions in a small ecosystem. Hydrobiologia 200/201: 275–289.Google Scholar
  102. Van Donk, E., M. P. Grimm, P. G. M. Heuts, G. Blom, K. Everards & O. F. R. van Tongeren, 1994a. Use of mesocosms in a shallow eutrophic lake to study the effects of different restoration measures. Arch. Hydrobiol. Beih. Ergebn. Limnol. 40: 283–294.Google Scholar
  103. Van Donk, E. & R. D. Gulati, in press. Transition of a lake to turbid state six years after biomanipulation: mechanisms and pathways. Wat. Sci. Tech.Google Scholar
  104. Van Donk, E., R. D. Gulati, A. Iedema & J. T. Meulemans, 1993. Macrophyte-related shifts in the nitrogen and phosphorus contents of the different trophic levels in a biomanipulated shallow lake. Hydrobiologia 251: 19–26.Google Scholar
  105. Van Liere, L., R. D. Gulati, F. G. Wortelboer & E. H. R. R. Lammens, 1990. Phosphorus dynamics following restoration measures in the Loosdrecht Lakes (The Netherlands). Hydrobiologia 191: 87–95.Google Scholar
  106. Werner, E. E., J. F. Gilliam, D. J. Hall & G. G. Mittelbach, 1983. An experimental test of the effects of predation risk on habitat use in fish. Ecology 64: 1540–1548.Google Scholar
  107. Winfield, I. J., 1986. The influence of simulated aquatic macrophytes on the zooplankton consumption rate of juvenile roach, Rutilus rutilus, rudd, Scardinius erythrophthalmus, and perch, Perca fluviatilis. J. Fish. Biol. 29: 37–48.Google Scholar
  108. Wium-Anderson, S., U. Anthoni, C. Christophersen & G. Houen, 1982. Allelopathic effects on phytoplankton by substances isolated from aquatic macrophytes (Charales). Oikos 39: 187–190.Google Scholar

Copyright information

© Kluwer Academic Publishers 1997

Authors and Affiliations

  • Martin R. Perrow
    • 1
  • Marie-Louise Meijer
    • 2
  • Piotr Dawidowicz
    • 3
  • Hugo Coops
    • 2
  1. 1.Department of Freshwater EcologyNERISilkeborgDenmark
  2. 2.RIZA, Institute for Inland Water management and Waste Water TreatmentLelystadThe Netherlands
  3. 3.Department of HydrobiologyUniversiy of WarsawWarszawaPoland

Personalised recommendations